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An inhibitory sex pheromone tastes bitter for Drosophila males.

Lacaille F, Hiroi M, Twele R, Inoshita T, Umemoto D, Manière G, Marion-Poll F, Ozaki M, Francke W, Cobb M, Everaerts C, Tanimura T, Ferveur JF - PLoS ONE (2007)

Bottom Line: In Drosophila melanogaster, as in many insects, cuticular hydrocarbons are thought to be involved in sex recognition and in mating behavior, but there is no direct neuronal evidence of their pheromonal effect.Cross-adaptation between Z-7-tricosene and bitter stimuli further indicates that these two very different substances are processed by the same neural pathways.Furthermore, the two substances induced similar behavioral responses both in courtship and feeding tests.

View Article: PubMed Central - PubMed

Affiliation: Université de Bourgogne, CNRS-UMR5548, Dijon, France.

ABSTRACT
Sexual behavior requires animals to distinguish between the sexes and to respond appropriately to each of them. In Drosophila melanogaster, as in many insects, cuticular hydrocarbons are thought to be involved in sex recognition and in mating behavior, but there is no direct neuronal evidence of their pheromonal effect. Using behavioral and electrophysiological measures of responses to natural and synthetic compounds, we show that Z-7-tricosene, a Drosophila male cuticular hydrocarbon, acts as a sex pheromone and inhibits male-male courtship. These data provide the first direct demonstration that an insect cuticular hydrocarbon is detected as a sex pheromone. Intriguingly, we show that a particular type of gustatory neurons of the labial palps respond both to Z-7-tricosene and to bitter stimuli. Cross-adaptation between Z-7-tricosene and bitter stimuli further indicates that these two very different substances are processed by the same neural pathways. Furthermore, the two substances induced similar behavioral responses both in courtship and feeding tests. We conclude that the inhibitory pheromone tastes bitter to the fly.

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7-T elicits a dose-dependent electrophysiological response in a subset of labial palp gustatory neurons.(A) Schematic illustration of the “tungsten electrod method” which allows simultaneous but separate stimulation and recording of gustatory and pheromonal stimuli. The stimulus was contained in a glass microelectrode capping the tip of the sensillum; caffeine and 7-T were dissolved in mineral oil, sucrose and salts were dissolved in water. Recordings were obtained from three types of labellar sensilla (l-, i- and s-type) determined according to both their location and shape [21]–[23] in wild-type Canton-S males. So far, we were unable to use this method to record from sensilla on the fore-tarsus, because of the relative hardness of the leg cuticle and the slender form of this appendage. (B) In i-type sensilla, one cell responded to 10−8M 7-T, whereas the second cell responded to 0.2 M NaCl. The shaded bar represents the duration of the stimulation (2 sec). Elicited spikes were separated according to spike height (amplitude of “class 0” and “class 1” were 0.3–0.5 mV and 0.1–0.2 mV, respectively); see left side of panel; n = 20 flies. (C) Conversely, l-type sensilla responded normally to NaCl, sucrose, KCl but not to 10−8M 7-T. Recording were made in similar conditions as described for i-type sensilla; n = 32 flies. (D) 7-T responsive sensilla were mapped on the labial palp with tungsten electrode recordings. Both i- and s-types-but no l-type—sensilla responded to stimulation with 7-T (a sensillum was considered as responsive if it showed at least one response to 7-T among 2-5 trials). Anterior is up, dorsal is right. GRN = gustatory receptor neuron; MR = mechanoreceptor neuron. (E) In a s-type sensillum (S2), the L2 cell showed a dose-dependent increased activity to 7-T (between 10−12 and 10−8M) while the L1 cells were not activated. Vertical axis: total number of spikes during 2 sec stimulation. Significantly increased activity of the L2 cell is indicated (a–b: p<0.05, a–c: p<0.01; n = 4–10).
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pone-0000661-g003: 7-T elicits a dose-dependent electrophysiological response in a subset of labial palp gustatory neurons.(A) Schematic illustration of the “tungsten electrod method” which allows simultaneous but separate stimulation and recording of gustatory and pheromonal stimuli. The stimulus was contained in a glass microelectrode capping the tip of the sensillum; caffeine and 7-T were dissolved in mineral oil, sucrose and salts were dissolved in water. Recordings were obtained from three types of labellar sensilla (l-, i- and s-type) determined according to both their location and shape [21]–[23] in wild-type Canton-S males. So far, we were unable to use this method to record from sensilla on the fore-tarsus, because of the relative hardness of the leg cuticle and the slender form of this appendage. (B) In i-type sensilla, one cell responded to 10−8M 7-T, whereas the second cell responded to 0.2 M NaCl. The shaded bar represents the duration of the stimulation (2 sec). Elicited spikes were separated according to spike height (amplitude of “class 0” and “class 1” were 0.3–0.5 mV and 0.1–0.2 mV, respectively); see left side of panel; n = 20 flies. (C) Conversely, l-type sensilla responded normally to NaCl, sucrose, KCl but not to 10−8M 7-T. Recording were made in similar conditions as described for i-type sensilla; n = 32 flies. (D) 7-T responsive sensilla were mapped on the labial palp with tungsten electrode recordings. Both i- and s-types-but no l-type—sensilla responded to stimulation with 7-T (a sensillum was considered as responsive if it showed at least one response to 7-T among 2-5 trials). Anterior is up, dorsal is right. GRN = gustatory receptor neuron; MR = mechanoreceptor neuron. (E) In a s-type sensillum (S2), the L2 cell showed a dose-dependent increased activity to 7-T (between 10−12 and 10−8M) while the L1 cells were not activated. Vertical axis: total number of spikes during 2 sec stimulation. Significantly increased activity of the L2 cell is indicated (a–b: p<0.05, a–c: p<0.01; n = 4–10).

Mentions: To investigate the role of gustatory neurons in detecting male inhibitory pheromones, we measured the electrophysiological activity of these neurons in response to pure synthetic 7-T. Our tungsten electrode method allowed us to separately stimulate and record the electrophysiological activity of a sensillum on the labial palp. The stimulating electrode was filled with a lipophilic buffer (paraffin oil) containing 7-T, and capped the tip of the taste sensillum, while the tungsten recording electrode was inserted at the base of the sensillum (Fig. 3A).


An inhibitory sex pheromone tastes bitter for Drosophila males.

Lacaille F, Hiroi M, Twele R, Inoshita T, Umemoto D, Manière G, Marion-Poll F, Ozaki M, Francke W, Cobb M, Everaerts C, Tanimura T, Ferveur JF - PLoS ONE (2007)

7-T elicits a dose-dependent electrophysiological response in a subset of labial palp gustatory neurons.(A) Schematic illustration of the “tungsten electrod method” which allows simultaneous but separate stimulation and recording of gustatory and pheromonal stimuli. The stimulus was contained in a glass microelectrode capping the tip of the sensillum; caffeine and 7-T were dissolved in mineral oil, sucrose and salts were dissolved in water. Recordings were obtained from three types of labellar sensilla (l-, i- and s-type) determined according to both their location and shape [21]–[23] in wild-type Canton-S males. So far, we were unable to use this method to record from sensilla on the fore-tarsus, because of the relative hardness of the leg cuticle and the slender form of this appendage. (B) In i-type sensilla, one cell responded to 10−8M 7-T, whereas the second cell responded to 0.2 M NaCl. The shaded bar represents the duration of the stimulation (2 sec). Elicited spikes were separated according to spike height (amplitude of “class 0” and “class 1” were 0.3–0.5 mV and 0.1–0.2 mV, respectively); see left side of panel; n = 20 flies. (C) Conversely, l-type sensilla responded normally to NaCl, sucrose, KCl but not to 10−8M 7-T. Recording were made in similar conditions as described for i-type sensilla; n = 32 flies. (D) 7-T responsive sensilla were mapped on the labial palp with tungsten electrode recordings. Both i- and s-types-but no l-type—sensilla responded to stimulation with 7-T (a sensillum was considered as responsive if it showed at least one response to 7-T among 2-5 trials). Anterior is up, dorsal is right. GRN = gustatory receptor neuron; MR = mechanoreceptor neuron. (E) In a s-type sensillum (S2), the L2 cell showed a dose-dependent increased activity to 7-T (between 10−12 and 10−8M) while the L1 cells were not activated. Vertical axis: total number of spikes during 2 sec stimulation. Significantly increased activity of the L2 cell is indicated (a–b: p<0.05, a–c: p<0.01; n = 4–10).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC1937024&req=5

pone-0000661-g003: 7-T elicits a dose-dependent electrophysiological response in a subset of labial palp gustatory neurons.(A) Schematic illustration of the “tungsten electrod method” which allows simultaneous but separate stimulation and recording of gustatory and pheromonal stimuli. The stimulus was contained in a glass microelectrode capping the tip of the sensillum; caffeine and 7-T were dissolved in mineral oil, sucrose and salts were dissolved in water. Recordings were obtained from three types of labellar sensilla (l-, i- and s-type) determined according to both their location and shape [21]–[23] in wild-type Canton-S males. So far, we were unable to use this method to record from sensilla on the fore-tarsus, because of the relative hardness of the leg cuticle and the slender form of this appendage. (B) In i-type sensilla, one cell responded to 10−8M 7-T, whereas the second cell responded to 0.2 M NaCl. The shaded bar represents the duration of the stimulation (2 sec). Elicited spikes were separated according to spike height (amplitude of “class 0” and “class 1” were 0.3–0.5 mV and 0.1–0.2 mV, respectively); see left side of panel; n = 20 flies. (C) Conversely, l-type sensilla responded normally to NaCl, sucrose, KCl but not to 10−8M 7-T. Recording were made in similar conditions as described for i-type sensilla; n = 32 flies. (D) 7-T responsive sensilla were mapped on the labial palp with tungsten electrode recordings. Both i- and s-types-but no l-type—sensilla responded to stimulation with 7-T (a sensillum was considered as responsive if it showed at least one response to 7-T among 2-5 trials). Anterior is up, dorsal is right. GRN = gustatory receptor neuron; MR = mechanoreceptor neuron. (E) In a s-type sensillum (S2), the L2 cell showed a dose-dependent increased activity to 7-T (between 10−12 and 10−8M) while the L1 cells were not activated. Vertical axis: total number of spikes during 2 sec stimulation. Significantly increased activity of the L2 cell is indicated (a–b: p<0.05, a–c: p<0.01; n = 4–10).
Mentions: To investigate the role of gustatory neurons in detecting male inhibitory pheromones, we measured the electrophysiological activity of these neurons in response to pure synthetic 7-T. Our tungsten electrode method allowed us to separately stimulate and record the electrophysiological activity of a sensillum on the labial palp. The stimulating electrode was filled with a lipophilic buffer (paraffin oil) containing 7-T, and capped the tip of the taste sensillum, while the tungsten recording electrode was inserted at the base of the sensillum (Fig. 3A).

Bottom Line: In Drosophila melanogaster, as in many insects, cuticular hydrocarbons are thought to be involved in sex recognition and in mating behavior, but there is no direct neuronal evidence of their pheromonal effect.Cross-adaptation between Z-7-tricosene and bitter stimuli further indicates that these two very different substances are processed by the same neural pathways.Furthermore, the two substances induced similar behavioral responses both in courtship and feeding tests.

View Article: PubMed Central - PubMed

Affiliation: Université de Bourgogne, CNRS-UMR5548, Dijon, France.

ABSTRACT
Sexual behavior requires animals to distinguish between the sexes and to respond appropriately to each of them. In Drosophila melanogaster, as in many insects, cuticular hydrocarbons are thought to be involved in sex recognition and in mating behavior, but there is no direct neuronal evidence of their pheromonal effect. Using behavioral and electrophysiological measures of responses to natural and synthetic compounds, we show that Z-7-tricosene, a Drosophila male cuticular hydrocarbon, acts as a sex pheromone and inhibits male-male courtship. These data provide the first direct demonstration that an insect cuticular hydrocarbon is detected as a sex pheromone. Intriguingly, we show that a particular type of gustatory neurons of the labial palps respond both to Z-7-tricosene and to bitter stimuli. Cross-adaptation between Z-7-tricosene and bitter stimuli further indicates that these two very different substances are processed by the same neural pathways. Furthermore, the two substances induced similar behavioral responses both in courtship and feeding tests. We conclude that the inhibitory pheromone tastes bitter to the fly.

Show MeSH
Related in: MedlinePlus